Holton was born in Oklahoma City. He graduated from Okmulgee High School in 1976. He attended Northeastern State University in Tahlequah, Oklahoma.
Holton's professional breakthrough came with the role of Francis Buxton, Pee-wee Herman's nemesis in the blockbuster comedy Pee-wee's Big Adventure (1985). He found further fame as high school basketball player Chubby in the werewolf comedies Teen Wolf (1985), and Teen Wolf Too (1987). His mainstream visibility grew with supporting roles in The Naked Gun: From the Files of Police Squad! (1988), A League of Their Own (1992), My Life (1993), and Little Giants (1994).
Holton has been equally prolific in television, performing in episodes of The Young and the Restless, Seinfeld, MacGyver, Sledge Hammer!, Tim and Eric Awesome Show, Great Job!, Star Trek: Deep Space Nine, NCIS, and NYPD Blue. He also makes an appearance in The Ramones' music video for "Something to Believe In". Following his cameo appearance in The Adventures of Rocky and Bullwinkle (2000), Holton refocused his attention on independent film and television projects. His first leading film role came through the direct-to-video drama Gacy (2003), in which he portrayed serial killer John Wayne Gacy.

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